Earth-Science Reviews 96 (2009) 163–172
Contents lists available at ScienceDirect
Earth-Science Reviews
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e a r s c i r ev
Flat laminated microbial mat communities
Jonathan Franks, John F. Stolz ⁎
Department of Biological Sciences, Duquesne University, Pittsburgh, PA 15282, United States
a r t i c l e
i n f o
Article history:
Received 28 January 2008
Accepted 24 October 2008
Available online 6 November 2008
Keywords:
microbial mat
oxygenic phototroph
anoxygenic phototroph
microbiolite
a b s t r a c t
Flat laminated microbial mats are complex microbial ecosystems that inhabit a wide range of environments
(e.g., caves, iron springs, thermal springs and pools, salt marshes, hypersaline ponds and lagoons, methane
and petroleum seeps, sea mounts, deep sea vents, arctic dry valleys). Their community structure is deﬁned by
physical (e.g., light quantity and quality, temperature, density and pressure) and chemical (e.g., oxygen,
oxidation/reduction potential, salinity, pH, available electron acceptors and donors, chemical species)
parameters as well as species interactions. The main primary producers may be photoautotrophs (e.g.,
cyanobacteria, purple phototrophs, green phototrophs) or chemolithoautophs (e.g., colorless sulfur oxidizing
bacteria). Anaerobic phototrophy may predominate in organic rich environments that support high rates of
respiration. These communities are dynamic systems exhibiting both spatial and temporal heterogeneity.
They are characterized by steep gradients with microenvironments on the submillimeter scale. Diel
oscillations in the physical-chemical proﬁle (e.g., oxygen, hydrogen sulﬁde, pH) and species distribution are
typical for phototroph-dominated communities. Flat laminated microbial mats are often sites of robust
biogeochemical cycling. In addition to well-established modes of metabolism for phototrophy (oxygenic and
non-oxygenic), respiration (both aerobic and anaerobic), and fermentation, novel energetic pathways have
been discovered (e.g., nitrate reduction couple to the oxidation of ammonia, sulfur, or arsenite). The
application of culture-independent techniques (e.g., 16S rRNA clonal libraries, metagenomics), continue to
expand our understanding of species composition and metabolic functions of these complex ecosystems.
© 2008 Elsevier B.V. All rights reserved.
Contents
1.
2.
Introduction . . . . . . . . . . . . . . . . . . .
Physical–chemical environment . . . . . . . . . .
2.1.
Light quantity and quality . . . . . . . . .
2.2.
Temperature . . . . . . . . . . . . . . .
2.3.
Oxygen . . . . . . . . . . . . . . . . . .
2.4.
pH . . . . . . . . . . . . . . . . . . . .
2.5.
Salinity . . . . . . . . . . . . . . . . . .
2.6.
Electron acceptors and donors, and chemical
3.
Community structure. . . . . . . . . . . . . . .
4.
Advances in techniques . . . . . . . . . . . . . .
5.
Summary . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
⁎ Corresponding author. Tel.: +1 412 396 6333; fax: +1 412 396 5907.
E-mail address: [email protected] (J.F. Stolz).
0012-8252/$ – see front matter © 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.earscirev.2008.10.004
Microbial mats are communities of microorganisms that colonize
surfaces. They range in complexity from simple, almost mono-species
bioﬁlms, to multi-layered ecosystems containing diverse populations of
prokaryotes and small eukaryotes (e.g., diatoms, unicellular algae)
164
J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172
arranged into assemblages and guilds (Stolz, 2000). Typically associated
with the sediment/water interface these communities interact with the
sediment, trapping and binding particles and clastics, and in some cases
inducing precipitation and lithiﬁcation (Stolz, 2003, Dupraz and Visscher,
2005). These activities in concert with the predominant mineralogy (e.g.,
clay, silt, siliciclastic, evaporite, carbonate) can impact the structure and
fabric yielding sediments with distinctive characteristics (e.g., microbiolites). The structures can be preserved in the rock record and their
interpretation can be enhanced by the study of modern microbiolites
(Grotzinger and Knoll, 1999; Des Marais, 2003; Tice and Lowe, 2004;
Noffke, 2007). Stromatolites and thrombolites are organosedimentary
structures that commonly have a vertical proﬁle that protrudes above the
horizontal plane (Monte, 1976; Reid et al., 1995, 2000). Flat laminated
microbial mats rarely form relief above the horizon (e.g., desiccation
cracks, Fig. 1), but the layered sediments they produce may extend to
some depth below the surface (e.g., a few centimeters to meters) (Figs. 1
and 2). They thrive in a wide range of habitats including extremes in pH
(e.g., acidic sulfur caves and iron springs), temperature (e.g., thermal
springs and pools, deep sea vents), and salinity (e.g., salt marshes,
hypersaline ponds and lagoons), as well as ones with chemolithotrophic
sources of energy (e.g., methane seeps, sea mounts). Their ecological
success is a reﬂection of the metabolic versatility and physiological
adaptability found within the Bacteria and Archaea. Flat laminated
microbial mats are models for microbial ecology and have been studied
extensively under the auspices of evolution and astrobiology as they
represent the modern analogs to ancient life and possibly extraterrestrial
ecosystems (Des Marais, 2003). Over the past twenty odd years several
volumes have been published dedicated to microbial mats (e.g., Cohen
et al., 1984; Cohen and Rosenberg, 1989 Stal and Caumette, 1994, Riding
and Awramik, 2000, Krumbein et al., 2003, Inskeep and McDermott,
2005a). The purpose of this review is to present a synopsis of the current
concepts, highlight some of the recent discoveries, and provide a glimpse
at what lies ahead with application of new technologies.
2. Physical–chemical environment
Fig. 1. Sippewissett Marsh, Massachusetts. A) Field photo facing westward, B) Close up
showing ﬂat laminated mat on surface.
Species occurrence and abundance in microbial mats are strongly
inﬂuenced by the physical properties and the chemical parameters of a
given environment. Important physical properties include light (both
quantity and quality), temperature, and pressure. Key chemical
Fig. 2. Flat laminated mat at Laguna Figueroa, Baja California, Mexico. A) Field photo facing eastward, B) Cross section of laminated sediments. The top 3 mm is the seasonal sediment
accreting community.
J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172
parameters include oxygen, pH, oxidation/reduction potential, salinity,
and available electron acceptors and donors, as well as the presence or
absence of speciﬁc chemical species. In this section, speciﬁc properties
and parameters that create unique environments that support microbial
mat communities are presented.
2.1. Light quantity and quality
Photoautotrophic communities depend on both the appropriate
amount of light (e.g., light quantity) and the particular wavelengths
(e.g., light quality) that can be used by the light harvesting pigments and
photosystems. The average amount of light that illuminates a surface on a
sunny day is 1000 to 2000 μE/m2/s. Depending on the environment,
however, light absorption and scattering can be signiﬁcant. Particles and
populations of organisms readily attenuate light in the water column.
Sediment type can impact the depth at which light can penetrate into the
subsurface. This light scattering can be signiﬁcant resulting in the scalar
irradiance being greater than the downward irradiance (Des Marais,
2003). Most phototrophs are adapted to low light intensities and often
are photoinhibited. The optimum light intensity for cyanobacteria in the
microbial mats of Mellum Island in the North Sea is 50 to 150 μE/m2/s.
Purple sulfur bacteria from the same mats use from 5 to 10 μE/m2/s (Stal
et al., 1985). Mat communities have a variety of strategies to obtain the
appropriate amount of light. Cyanobacteria produce carotenoids and
other light attenuating products (e.g., scytonemin), or may lie beneath a
coating of sediment (Palmisano et al., 1989). Conversely, some phototrophs are extremely adept at capturing rare photons in light-limited
environments. Bacteriochlorophyll e containing green sulfur bacteria
have been found at 100 m depth in the Black Sea (Manske et al., 2005).
Green sulfur bacteria are particularly well suited for low light as they can
produce large numbers of light harvesting structures (e.g., chlorosomes)
and have a high ratio of accessory pigment to reaction center (Jochum
et al., 2008). The Black Sea chlorobia, for example, are capable of
photoautotrophy with only 0.015 μmol quanta m− 2 s− 1 (Manske et al.,
2005). Geographic location can be important with respect to the growing
season of mats. While equatorial mats see little annual change, northern
and southern latitudes are subject to seasonality, while artic and Antarctic
systems are subject to month long extremes of constant light or darkness.
Phototrophic organisms have evolved light harvesting structures and
photosystems that utilize different wavelengths of light. Cyanobacteria
have thylakoids with chlorophyll a (680 nm) and phycobilins (e.g.,
phycoerythrin, phycocyanin), green phototrophs have chlorosomes
with bacteriochlorophyll c (740 nm), d (725 nm), or e (714 nm), and
purple phototrophs have intracytoplasmic membranes with either
bacteriochlorophyll a (800–890 nm) or bacteriochlorophyll b
(1015 nm) (Stolz, 2007). These different photosystems allow a variety
of phototrophic microorganisms to coexist, often forming distinct guilds
and assemblages. Water is a natural attenuator of light, absorbing most
of the infrared wavelengths within the ﬁrst meter. Paradoxically, it is the
longer wavelengths that penetrate further into shallow water sediments
(Jørgensen and Des Marais, 1986; Jørgensen et al., 1987; Pierson et al.,
1987; Polerecky et al., 2007). Thus anoxygenic green and purple
phototrophs can predominate certain layers (Fig. 3) and make a
signiﬁcant contribution to the biomass and primary productivity of
the mat (D'Amelio et al., 1987; Stolz, 1990; Nuebel et al., 2001; Polerecky
et al., 2007). Flat laminated mats found in very shallow pools, lagoons,
and salt marshes often have a distinct layer of anoxygenic purple
Fig. 3. Community structure in the ﬂat laminated microbial mat from Laguna Figueroa,
Baja California, Mexico. A) Surface 0–1 mm showing bundles of ﬁlaments of Microcoleus
chthonoplastes. B) Subsurface 1–2 mm showing ﬁlaments of M. chthonoplastes and
Chloroﬂexus-like ﬁlamentous green bacterium. C) Subsurface 2–3 mm with Chloroﬂexuslike ﬁlamentous green bacterium. Samples were glutaraldehyde ﬁxed (2.5% in seawater
buffer) and observed by Confocal Scanning Laser Microscopy (Leica TCS SP2), with
excitation at 488 nm and emissions at 644–722 nm and 507–536 nm. (C) Chloroﬂexus-like
ﬁlamentous green bacterium, (M) M. chthonoplastes, (N) nematode. All ﬁgures have the
same magniﬁcation, bar 20 μm.
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J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172
phototrophs with bacteriochlorophyll b below layers of cyanobacteria,
and purple and green phototrophs (Nicholson et al., 1987; Pierson et al.,
1987; Stolz, 1990).
2.2. Temperature
Microbial mats have been found in the frozen Antarctic (Priscu et al.,
1998; Taton et al., 2003; Jungblut et al., 2005), as well as by hot springs
(Ward et al., 1998; Roeselers et al., 2007) and thermal vents (Alain et al.,
2004; Nakagawa et al., 2005). Psychrophiles, organisms adapted to
extreme cold, are often oligotrophic, living on trace nutrients, and
having long generation times. Hot springs provide a temperature range
from boiling at the source (100 °C at sea level, slightly lower, ~92 °C, at
higher elevations) to ~40 °C down stream with different microbial
populations existing along the gradient. The temperature of water
ﬂowing from a deep sea thermal vent may exceed 400 °C as it is under
extreme pressure (Zierenberg et al., 2000). Nevertheless, physiologically
diverse Archaea and Bacteria exist at elevated temperatures and
extensive microbial mats can develop, supported by chemolithoautotrophy. The organisms associated with thermal springs and vents are
distributed based on their temperature optimum, and ecotypes of the
same species may exist at different temperatures (Ward et al., 2006;
Bhaya et al., 2007). While photosynthesis seems to be limited to
temperatures below 75 °C (Madigan, 2003), sulfur, iron, and nitrogen
metabolism can occur at higher temperatures (Stetter, 1999, Ferrera and
Reysenbach, 2007). The current record for nitrogen ﬁxation is 92 °C, by a
thermal vent methanogen (Mehta and Baross, 2006). The community
composition in thermal environments are also impacted by pH, and
chemical species such as iron, sulfur, chloride, and arsenic (Pierson et al.,
1999, Skirnisdottir et al., 2000; Inskeep and McDermott, 2005b; Inskeep
et al., 2007).
2.3. Oxygen
Flat laminated microbial mats are often the sites of steep oxygen
gradients that can transition from supersaturation (N500 μM), just
below the sediment/water interface, to total anoxia within less than a
millimeter (Dupraz and Visscher, 2005). Diffusion of oxygen from the
overlying water column, in situ oxygenic photosynthesis, aerobic
respiration and sulﬁde production (by sulfate reducing bacteria)
principally determine the depth proﬁle of the oxic/anoxic transition
zone (OATZ) (Canﬁeld and Des Marais, 1993). The proﬁle usually
follows a diurnal pattern in which the greatest net oxygen production
occurs in the middle of the day (Visscher et al., 1998) (Fig. 4). There
are cases, however, in which the peak is in late morning as the
intensity of the noon-day sun can inhibit photosynthesis (Miller et
al., 1998, Jonkers et al., 2003). Typically, the oxygen concentration in
the surface of the mat is at equilibrium with the overlying water
column but increases with depth in the ﬁrst few millimeters, then
rapidly decreases. At night, a combination of respiration and
sulﬁdogenesis combine to move the OATZ closer to the surface. This
diel shift is often accompanied by the movement of motile microbial
species (e.g., Beggiatoa sp.) in response to the change (Hinck et al.,
2007). The activity of the oxygenic phototrophs (e.g., cyanobacteria)
can also affect the oxidation reduction potential (Eh) of the sediment,
resulting in Eh values as high as 400 mV in the oxic zone (Visscher
and Stolz, 2005).
2.4. pH
The pH of the environment can have an impact on microbial
community composition as it affects an organism's cell wall integrity,
and the ability to produce energy as well as obtain certain nutrients.
Oxidative phosphorylation is dependent on proton motive force, and
both acidophiles and alkaliphiles have adaptations to deal with the
extremes in external hydrogen ion concentration and internal pH
(Krulwich et al., 1996). Nutrient transport may be charge dependent
and thus subject to the pH of the environment. Nevertheless,
microbial mats have been found to thrive in the extreme low pH of
acid mine drainage (Bond et al., 2000a,b; Baker and Banﬁeld, 2003)
and acid sulfur springs (Meisinger et al., 2007), as well as the elevated
pH of silicious hot springs (Nakagawa and Manabu, 2002; van der
Meer et al., 2000, 2005) and high pH (9–10) of alkaline lakes. To date,
the most extreme appears to be the microbial mats of Iron Mountain,
with a pH of below 1 (Baker and Banﬁeld, 2003). As might be
expected, the microbial diversity, based on 16S rRNA gene sequences,
is quite limited to mostly species of Leptospirillum and Ferromicrobium
(Bond et al., 2000b), with some Acidomicrobium and unidentiﬁed
proteobacteria and Thermoplasmales as well (Bond et al., 2000a). Even
in environments where the pH of the overlying water is near neutral,
the metabolic activity of the different guilds can result in a pH gradient
(Fig. 4). Oxygenic photosynthesis can raise the pH in excess of 9, while
fermentation and anaerobic respiration can lower the pH to below 6.8
(Revsbech et al., 1983).
2.5. Salinity
Fig. 4. Idealized proﬁles for oxygen, sulﬁde, and pH during the day (light) and night
(dark) (modiﬁed from Dupraz and Visscher, 2005).
The presence of dissolved soluble salts affects both the density
and the chemical activity of water. The effect of salinity upon osmotic
potential is particularly important from a biological perspective.
Organisms living in marine and hypersaline environments are
hypotonic with a cytoplasm less saline than the surrounding water.
To counteract the tendency for water to leave the cell osmolites such
as glycerol and glycine-betaine act as compatible solutes, creating an
apparent osmotic potential equal to the external environment.
Freshwater organisms are faced with the opposite problem. They
are hypertonic and their cytoplasm is less dilute than their
surroundings, thus water has a tendency to enter the cell. However,
the difference is not as great as that facing marine organisms and
water is regulated by active diffusion out of the cell. Most eukaryotic
organisms can't handle either high salt or exposure to extreme
oscillations in salinity. Thus ﬂat laminated microbial mats often
ﬂourish in intertidal ﬂats and hypersaline lagoons (Nicholson et al.,
1987; Stolz, 1990; Des Marais, 2003; Bachar et al., 2007). The tidal
J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172
changes in salinity that particularly occur in the intertidal zone affect
the microbial diversity, photosynthesis and respiration (Raeid et al.,
2007).
2.6. Electron acceptors and donors, and chemical species
Microbial mats can be considered natural bioreactors as they are
often the site of intense biogeochemical cycling (Visscher and Stolz,
2005). They can provide nitrogen and carbon, and produce signiﬁcant
amounts of H2 and CO, as well as methane (Pearl et al., 2000; Hoehler
et al., 2001). Energy generation and acquisition of essential elements
drive the transformation of chemical species. Thus the chemical
proﬁle primarily reﬂects the metabolic activity of the guilds and
assemblages, but is also inﬂuenced by abiotic factors. Energy and
carbon are provided by the autotrophic members of the community.
These include oxygenic photolithoautotophs (e.g., diatoms, cyanobacteria), anoxygenic photolithoautotrophs (e.g., purple sulfur
bacteria, green sulfur bacteria), anoxygenic photoorganotrophs
(e.g., purple bacteria, green ﬁlamentous bacteria), and chemolithoautotrophs (e.g., iron oxidizing bacteria, sulfur oxidizing bacteria, nitrifying bacteria, methylotrophs). The carbon in turn may be
oxidized back to CO 2 through respiration (both aerobic and
anaerobic) and fermentation. Respiration requires the availability
of electron acceptors, that in coupled reactions, oxidize the organics
(e.g., electron donors). The canonical progression of electron
acceptors, as predicted by thermodynamic considerations, is O2 →
+4
NO−
→ Fe+3 → SO−2
→ CO2. Thus one would expect the
3 → Mn
4
dominant process to proceed, from surface to depth, aerobic
respiration, nitrate reduction (e.g., denitriﬁcation), manganese
reduction, iron reduction, sulfate reduction, then methanogenesis.
However, studies on ﬂat laminated mats (Canﬁeld and Des Marais,
1991) and stromatolites (Visscher et al., 1998), have shown active
sulfate reduction at or near the surface in the zone of oxygenic
photosynthesis. In microbial ecosystems where light is not available
(e.g., caves, deep sea), chemolithoautotrophy provides the bulk of the
energy and carbon. Deep sea thermal vents and sulfur caves have
communities dominated by sulfur oxidizing epsilonproteobacteria
(Engel et al., 2003, 2004; Alain et al., 2004; Nakagawa et al., 2005,
2006). Cold methane seeps support communities of methylotrophs
and sulfur oxidizers (Michaelis et al., 2002; Reitner et al., 2005;
Arakawa et al., 2006). Interestingly, the methane oxidation is an
anaerobic process and two groups of Archaea (ANME-1, ANME-2)
have been identiﬁed that can couple the reduction of sulfate to the
oxidation of methane (Michaelis et al., 2002; Treude et al., 2003). The
Black Sea microbial mats were shown to simultaneously consume
methane and sulfate with the population dominated by ANME-1 type
methylotrophs (Treude et al., 2005). More recently, the involvement
of methyl sulﬁdes in anaerobic methane oxidation has been reported
(Moran et al., 2008). Iron oxidizing chemolithoautotrophs support
communities in both marine such as the iron-rich mats of the Loihi
Seamount (Gao et al., 2006) and terrestrial such as Iron Mountain
(Bond et al., 2000a,b; Baker and Banﬁeld, 2003).
Microbial mats of ﬁlamentous chemolithoautotrophic sulfuroxidizing bacteria (e.g., Beggiatoa spp., Thioploca spp., Thiomargarita
namibiensis) have been found on surface sediments from coastal zones
(e.g., Santa Barbara Basin), upwelling zones, cold seeps, methane
seeps, deep sea vents and mud volcanos (Mills et al., 2004; de Beer
et al., 2006, Hinck et al., 2007; Preisler et al., 2007). The size of the
individual ﬁlaments may be quite large, as they can be up to 10 μm in
diameter and hundreds of microns in length (Gallardo and Espinoza,
2007). Although known primarily for their ability to oxidize sulﬁde
with oxygen, some species can store nitrate intracellularly (Jørgensen
and Gallardo, 1999; Schulz et al., 1999) and are capable of using nitrate
as the electron acceptor (Hinck et al., 2007). The diel migration of
Beggiatoa and Thiovulum species in response to oxygen and sulﬁde
gradients has been known for some time (Jørgensen and Revsbech,
167
1983) but the accumulation of nitrate for later use in sulﬁde oxidation
was documented only recently.
There have been new discoveries about the ecological impact of
alternative electron donors and acceptors. For example, arsenic is readily
cycled in hypersaline environments and in the absence of signiﬁcant
sulfate reduction, drives the ecology (Oremland et al., 2005a). More
recently, arsenic has been directly linked to photoautotrophy in bioﬁlms
from Mono Lake CA, with As(III) being used as an electron donor in the
place of water or hydrogen sulﬁde (Kulp et al., 2008). Considering that
early microbial communities inhabited thermal and brine environments, where arsenic should be abundant, one may speculate that these
systems were fueled in part by arsenic cycling. Indeed, active arsenic
cycling has been demonstrated for several hot spring mat communities
(Inskeep et al., 2007). The versatility of nitrate as a terminal electron
acceptor has been expanded with the discovery of organisms that couple
nitrate reduction to the oxidation of sulfate (as described above),
arsenite (Oremland and Stolz, 2003), and ammonia, the latter being
known as “annamox” (Strous et al., 1999; Kuypers et al., 2003; Penton
et al., 2006).
3. Community structure
Community structure is the species composition (occurrence and
abundance) down the vertical proﬁle deﬁned within a network of
biogeochemical interactions. A microbial mat can be composed of
hundreds to thousands of species of organisms that are stratiﬁed into
a number of layers (Cohen et al., 1977; Stolz, 1983; DesMarais et al.,
1992; Ward et al., 1992; Castenholz, 1994; Ramsing et al., 2000; Stolz,
2000, 2003). Primarily comprised of bacteria and some Archaea,
eukaryotic organisms (e.g. diatoms) may also be signiﬁcant (Bonny
and Jones, 2007a,b). A variety of traditional techniques such as light
and ﬂuorescence microscopy, scanning and transmission electron
microscopy, have been used for species identiﬁcation (Stolz, 1994,
Stolz et al., 2001). Flat laminated microbial mats are no different than
most of the other microbial systems, in that “99%” of the species are
unculturable. More recently culture independent methods (e.g.,
molecular approaches discussed below) have been used to investigate
species diversity (Jonkers et al., 2003; Martínez-Alonso et al., 2005;
Baumgarter et al., 2006; Bachar et al., 2007). The microbial mats at
Guerrero Negro, for example, generated more than 1500 16S rRNA
sequences representing over 750 species (Ley et al., 2006). Certain key
species, especially phototrophs, can be readily identiﬁed in situ by
their ultrastructure (Stolz, 1983) (Fig. 3). Three examples of stratiﬁed
microbial communities are discussed below to demonstrate ecosystem dynamics.
The sandy mat of the Great Sippewissett Marsh, Cape Cod,
Massachusetts is an example of a stratiﬁed microbial community
(Nicholson et al., 1987). The mat is subject to the alternating tides,
being submerged at high tide and exposed at low tide. Gradients of
light, oxygen, and sulﬁde deﬁne the vertical proﬁle. The community
lies just below a surface layer of sand and has up to six layers
consisting of different microbial communities based on light and
electron microscopy observations. These layers are discernable
because of the different populations of pigmented organisms. The
uppermost layer is yellow in color due to the presence of diatoms and
a high concentration of carotenoids (Pierson et al., 1987). The next
layer is green because of the presence of cyanobacteria such as Oscillatoria sp. and Lyngbya estuarii. The third layer is pink in color and is
populated by purple sulfur bacteria (e.g., Amoebobacter sp., Thiocapsa
roseopersarcina). The oxygen concentration in the green layer is at
supersaturation because of active photosynthesis by the cyanobacteria. The pink layer, however, is anoxic, due to the combination of
high rates of respiration and sulfate reduction. The subsequent layers
are also dominated by anoxygenic phototrophic bacteria (e.g., purple
and green phototrophic bacteria). The fourth layer is salmon in color
due to the presence of purple sulfur bacteria with bacteriochlorophyll
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b (e.g., Thiocapsa pfennigii). The olive or ﬁfth layer is composed
primarily of the bacteriochlorophyll c containing green sulfur bacteria
(e.g., Prosthecochloris estuarii), and is underlain by a black, sulfurous
layer.
The above description is an oversimpliﬁcation and may give the
impression that these mat communities are a static system. Microbial
ecosystems are truly dynamic and can change dramatically over short
time periods. These changes can be brought about by active motility as
well as rapid growth. Microbes can cover great distances at speeds up
to hundreds of microns per second propelled by ﬂagella, gliding
motility, or other means. There are purple sulfur bacteria in the pink
layer of the Sippewissett sandy mat that have gas vacuoles (Nicholson
et al., 1987). Filaments of the sulfur oxidizing bacterium Beggiotoa sp.,
are known to migrate several centimeters through sediment during
the course of a night via gliding (Jørgensen and Revsbech, 1983;
Moeller et al., 1985; Hinck et al., 2007). The growth of microorganisms
can also be a factor. With generation times as brief as 20 min, massive
blooms of organisms can occur virtually overnight.
Catastrophic events in which a community or ecosystem is close to
or completely destroyed eventually lead to recolonization. The
phenomenon of succession in microbial ecosystems occurs in much
the same way that has been described for terrestrial ecosystems. Two
studies on stratiﬁed microbial communities, one on Mellum Island in
the North Sea, and the other in Laguna Figueroa, Baja California,
Mexico, provide insight into how such succession occurs.
The island of Mellum is a small uninhabited island in the southern
North Sea. Microbial mats are found in the upper intertidal zone and are
especially well developed on the western shore. Three different mat
types have been described (Stal et al., 1985). The microbial community
in the newly colonized sand is comprised mostly of Oscillatoria sp. with
lesser populations of Spirulina sp. and coccoid cyanobacteria. Essentially,
this community begins to produce the organics and ﬁx the nitrogen
necessary to support a community of greater complexity. A more
cohesive mat is dominated by the ﬁlamentous cyanobacterium Microcoleus chthonoplastes. M. chthonoplastes is easily recognized by the
bundle of ﬁlaments in a common sheath. The third microbial mat type
shows three layers, a surface green layer, dominated by ﬁlamentous
cyanobacteria (M. chthonoplastes, Oscillatoria sp.), a red layer, dominated
by purple sulfur bacteria (Thiocapsa sp., Thiopedia sp., Chromatium sp.,
Ectothiorhodospira sp.), and an underlying black layer, indicative of the
activity of sulfate reducing bacteria. The growing period for the mats
begins in May or June and ends in October or November. During the
winter they are often destroyed or greatly reduced in size. Growth
begins again in the spring with the colonization of the pristine sand with
ﬁlaments of the nitrogen ﬁxing Oscillatoria sp. (Stal et al., 1985).
Laguna Figueroa is a small hypersaline lagoon on the Paciﬁc Ocean
side of Baja California, del Norte (Fig. 2). Several different mat types can
be found (Margulis et al., 1980; Stolz, 1990). Only those mats that are
dominated by M. chthonoplastes, however, form laminations in the
sediment (Stolz, 1983; Stolz, 1990). Another distinguishing feature of
this mat is that it has four distinct layers each representing different
communities of phototrophic bacteria with keystone species: a surface
yellow layer with mostly diatoms and the cyanobacteria Phormidium sp.
and Aphanothece sp., a green layer with M. chthonoplastes and Chroococcidiopsis sp., a red layer with anoxygenic ﬁlamentous purple bacteria
(Chromatium sp., Thiocapsa roseoparsarcina) and a Chloroﬂexus-like
organism, and a salmon layer with Thiocapsa (Stolz, 1990; Fig. 3). The
mats at Laguna Figueroa are usually only ﬂooded for short periods each
spring. However, starting in 1979, corresponding with an unusually wet
winter caused by a strong el Niño, the lagoon ﬁlled up with over 3 m of
fresh water and 10 cm of terrigenous sediment, virtually burying the
community. Although the previously deposited laminated sediment
remained intact, the microbial mat that formed them was destroyed.
Once the waters receded, a thin veneer of halite covered the surface,
beneath which was a yellow layer of diatoms, and a thin green layer of
cyanobacteria (Oscillatoria salina, Spirulina subsalsa). The underlying
terrigenous sediment was also being reworked by heterotrophic
bacteria into a black ooze that reeked of hydrogen sulﬁde. After the
third summer, M. cthonoplastes returned to dominate the surface
community. Initially there was a thick gelatinous surface layer containing bundles of M. cthonoplastes, intermingled by ﬁlaments of S. subsalsa
and O. salina. Later a three layered mat developed. The yellow surface
layer was comprised mostly of diatoms (e.g., Navicula sp. Neitzche sp.,
Rhopolodia sp.), but had bundles of M. cthonoplastes, trichomes of
Phormidium sp., O. salina, and S. subsalsa, as well as clusters of Aphanothece sp., and Gleocapsa sp.. The second layer, green in color, was
dominated by the colonial coccoid Chroococcidiopsis. sp. and was
underlain by a black sulfurous mud. Although purple sulfur bacteria
were observed, no distinct layer was formed. At this point, the formation
of annual laminations resumed. It took almost four years, however, for
the full compliment of layers (yellow, green, red, salmon, and black) to
reappear. Diatoms dominated the yellow layer, M. cthonoplastes and
Chroococcidiopsis sp., the green layer, Chromatium sp. and the green
bacterium Chloroﬂexus sp. in the red layer, and T. pfennigii in the salmon
layer. Still some species were missing.
These last two examples provide an interesting contrast even though
they share similarities. The island of Mellum lies at 60° north latitude,
and the mats are seasonally destroyed. The communities are dominated
by rapid growing, upwardly mobile species and are reestablished every
year. Laguna Figueroa on the other hand, is in a subtropical climate, just
above 30° north latitude. Although the ﬂat laminated mats have an
annual growing season, the community is usually not destroyed by the
spring high tides. Thus species with less tolerance for perturbation or
slower growth kinetics may be able to persist. For this community, then,
the periodic ﬂooding and burial by terrestrial sediment has a greater
impact on the community structure. The fact that a community is
destroyed frequently does not necessarily mean the species diversity will
be any less, but rather that there is selective pressure for rapidly growing
species. The mats of Great Sippewissett Marsh, like the ones of the island
of Mellum, are destroyed every winter and yet they develop into a
multilayered community. This phenomenon is a reﬂection of the concept
that organisms with short generation times can potentially respond to
environmental changes with expediency, whereas organisms with long
generation times may take a greater time to respond, but may also persist
long after the optimal conditions for their growth have disappeared.
4. Advances in techniques
The application of molecular approaches to the study of microbial
ecology has revolutionized the ﬁeld (Oremland et al., 2005b). Initial
studies using dot blot hybridization and limited sequencing (Risatti et
al., 1994), have given way to large scale sequencing (Ward et al., 2006;
Baumgartner et al., 2006), gene expression studies (Steunou et al.,
2006), and metagenomic analysis (Bhaya et al., 2007). Volumes of 16S
rRNA gene sequences are now available through NCBI (http://www.ncbi.
nlm.nih.gov/) and the Ribosomal Database Project II (http://rdp.cme.
msu.edu/). Examples of phylogenetic studies based on 16S rRNA gene
sequences include intertidal mats (Rothrock and García-Pichel, 2005),
hypersaline mats (Risatti et al., 1994; López-Cortéz et al., 2001; Nuebel
et al., 2001; Casamayor et al., 2002; Jonkers et al., 2003; Sørenson et al.,
2005; Baumgartner et al., 2006), hot springs (Ruff-Roberts et al., 1994;
Ferris and Ward, 1997; Ferris et al., 1997; Jackson et al., 2001; Ferris et al.,
2003; Lacap et al., 2007; McGregor and Rasmussen, 2008), caves
(Holmes et al., 2001; Engel et al., 2003, 2004), arctic hot springs
(Roeselers et al., 2007), Antarctic lake mats (Taton et al., 2003; Jungblut
et al., 2005), benthic lakes (Koizumi et al., 2004), thermal vents (Alain
et al., 2004; Nakagawa et al., 2005, 2006), methane seeps (Michaelis
et al., 2002; Treude et al., 2003, 2005), and the microbial community
associated with coral black band disease (Barneah et al., 2007). These
studies have identiﬁed the major phylotypes and when done quantitatively, the dominant species. They have reinforced the idea that
microbial mats have great species richness and are organized into
J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172
guilds and assemblages (Ward et al., 2006). The phylogenic analyses can
also reveal historic features. The microbial community in Cuatro
Cienegas basin still maintains its marine heritage (50% of the phylotypes
are more closely related to marine species) even though the organisms
have not seen seawater since the Jurassic (Souza et al., 2006).
Conversely, ampliﬁcation and sequencing of ribosomal genes from a
217,000 year old Mediterranean sapropels identiﬁed phylotypes of
freshwater green sulfur bacteria (Coolen and Overmann, 2007). Other
studies have probed for speciﬁc groups with targeted primers for 16S
rRNA genes (or the 16S–23S intergenic region, Leuko et al., 2007) or
functional genes such as those involved in nitrogen ﬁxation (Moisander
et al., 2006), sulfate reduction (Dillon et al., 2007), and arsenite oxidase
(Inskeep et al., 2007). In some cases the phylogeny obtained from the
functional genes parallels that of the 16S rRNA gene, such as the Fenner–
Matthews–Olson protein in green sulfur bacteria (Alexander and Imhoff,
2006). This approach, however, is not a panacea, as there are examples
where the dominant phylotype has no known cultured relative. In
addition, the techniques are dependent on proper sample collection and
efﬁcient nucleic acid extraction. Flash freezing is often used in sample
collection, however, certain organisms readily lyse and their DNA is
degraded in the process (Giacomazzi et al., 2005; Suomalainen et al.,
2006), Conversely, some organisms are recalcitrant to cell lysis, and
nucleic acid extraction and ampliﬁcation from natural samples can be
hampered by the chemical composition and presence of organics (as
reviewed in Bertrand et al., 2005; Desai and Madamwar, 2007).
Therefore, when characterizing a new community, a variety of methods
should be tested, and the extraction efﬁciency determined.
There are now over 800 bacterial and 50 archaeal genomes being
sequenced or completed. This information has facilitated the application
of comparative genomics (Klatt et al., 2007), functional gene arrays
(Ward et al., 2007), and metagenomics (Ward et al., 2006; Wegley et al.,
2007) to probe functionality and diversity. In hot spring populations in
Mushroom Spring (Yellowstone National Park), ecotypes of different
Synecococcus have been recognized (Ward et al., 2006). M. chthonoplastes that has been found in ﬂat laminated mats across the globe are
morphologically and ultrastructurally identical, but it is questionable
whether they are all the same species or exhibit genetic variability and
distinct physiology depending on the environment. A recent study used
three gene loci on strains of M. chthonoplastes isolated by micromanipulation. The results seemed to indicate that there is indeed genetic
diversity in populations collected from the ten sites from three different
locations investigated (Lodders et al., 2005). Use of genome sequence
from pure cultures and metagenomic data from mixed populations will
allow for further investigation of the capabilities and interactions
between the microbial species in these mat communities. Thus efforts to
isolate and cultures organisms of interest as well as physiological and
biochemical studies must continue along side the molecular based
approaches (Wieringa et al., 2000; Oremland et al., 2005b).
Even microscopy has seen innovation with the development of the
ﬁeld emission gun environmental SEM (FEG-SEM) that allows for
examination of cryoﬁxed hydrated samples under low vacuum (Dupraz
et al., 2004). Confocal Laser Scanning Microscopy is quite useful for
detecting microbes that are autoﬂuorescent (e.g., phototrophic bacteria)
and can be expanded through the use of a wide range of new ﬂuorescent
stains and speciﬁc molecular probes (e.g. ﬂuorescence in situ hybridization, FISH). The sensitivity of FISH has been expanded through the use of
catalyzed reporter deposition (CARD-FISH) that ampliﬁes the signal
intensity of the probe (Schmid et al., 2006). Species identiﬁcation and
enzymatic activity can be accomplished by coupling of FISH with
microautoradiography (MAR-FISH) (Ouverny and Fuhrmann, 1999).
A novel approach to targeting speciﬁc species is stable isotope
probing (SIP). In this case, a substrate is labeled with 13C. The substrate is
then fed to the community and allowed to be metabolized with the label
eventually being incorporated into the cells' nucleic acids. The DNA and
RNA are then extracted and the “heavier” nucleic acids (those from
organisms that incorporated the 13C) are separated using density
169
gradient centrifugation. The 16S rRNA genes can then be ampliﬁed and
sequenced, and a species identiﬁcation made (Schmid et al., 2006).
Fatty acid and pigment determination have also been useful tools for
investigating community composition (Büehring et al., 2005; Nakajima
et al., 2003). More recently, environmental proteomics has become a
rapidly evolving ﬁeld. Based on the every increasing database of protein
sequences and their mass ﬁngerprint (after trysin digest), protein
fragments isolated from environmental samples can be identiﬁed using
mass spectrometry (Maldi-TOF and MS-MS analysis) (Ram et al., 2005).
5. Summary
Any given environment, whether aquatic or terrestrial, may be
deﬁned by a set of physical properties and chemical characteristics. The
physical properties are typically determined by abiotic processes while
the chemical characteristics may be markedly affected by the activity of
organisms. The distribution of phototrophic bacteria is primarily
determined by light, oxygen, and hydrogen sulﬁde. The quantity and
quality of the light is affected by the light attenuating properties of
water, but also by absorption by the different types of phototrophic
bacteria. The concentration of oxygen is affected by diffusion and mixing
as well as production by oxygenic phototrophs. The concentration of
sulﬁde is dependent on a source of sulfate, the activity of sulfate
reducing bacteria, and sulﬁde diffusion and consumption. These
interactions result in dynamic systems that can exhibit both spatial
and temporal heterogeneity, and provide a wide variety of environments
supporting a rich diversity of species. The application of culture
independent methods including metagenomics, will provide new
insight into the community structure and dynamics of ﬂat laminated
mats. Nevertheless, physiological and biochemical studies remain
essential for exploring the remarkable metabolic diversity and function
of the microbial species that inhabit these important ecosystems.
Acknowledgements
This work was supported in part by NSF grant EAR 0221796. The
authors wish to thank the members of the Research Initiative for
Bahamian Stromatolites for fruitful discussions. RIBS contribution #45.
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